Scientific Correspondence
Mutant Flower Morphologies in the Wind Orchid,
a Novel Orchid Model Species1
Sascha Duttke2, Nicholas Zoulias, and Minsung Kim*
Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, United Kingdom
Orchids comprise one of the largest and most diverse angiosperm families. Currently, about 24,500
orchid species have been reported, and there are
many more to be discovered (Dressler, 2005). Due to
their biological complexity, orchids have been proposed as an attractive system with which to address
many fundamental biological questions (Tupac Otero
et al., 2002; Cozzolino and Widmer, 2005; Dressler,
2005). In particular, orchid flowers are one of the best
examples of coevolution between plants and pollinators and thus provide a unique opportunity to study
development and evolution of flower forms and pollination biology. Highly modified flowers, selected for
deceiving pollinators, are seen in approximately onethird of all orchid species (Cozzolino and Widmer,
2005; Tremblay et al., 2005), and the floral complexity
of orchids has been proposed as one of the key factors
behind their rapid species radiation (Gill, 1989). The
orchid clade is also phylogenetically important, representing a petaloid monocot group that is distinct
from other model species, e.g. maize (Zea mays), snapdragon (Antirrhinum majus), and Arabidopsis (Arabidopsis thaliana). However, despite their apparent
importance, molecular and genetic approaches to orchid flower development and evolution are still in
their infancy. To date, orchids remain underrepresented in studies at a molecular level (Dressler, 1981;
McCook and Bateman, 1990; Peakall, 2007). One of the
main obstacles is the availability of a suitable model
species that is easy to maintain under laboratory
conditions and has a wide range of mutants. Here,
we report a mutant collection of the wind orchid
(Neofinetia falcata) as a powerful tool to study orchid
flower development. We also propose the wind orchid
as an orchid model species with enormous advantages
over other orchid species, which will answer biological
questions unique to orchids as well as questions of
plant evolution and development in broad terms.
AN OLD WIND ORCHID MUTANT COLLECTION
In far eastern Asian countries such as Korea, China,
and Japan, growing orchids has a long history. Over
1
This work was supported by the Royal Society (grant no.
RG2009/R111035).
2
Present address: Section of Molecular Biology, University of
California at San Diego, La Jolla, CA 92093.
* Corresponding author; e-mail [email protected].
www.plantphysiol.org/cgi/doi/10.1104/pp.111.191643
1542
the centuries, thousands of mutants and varieties of
native orchids have been collected from their natural
habitats. The wind orchid is one such orchid, the
cultivation of which was recorded as early as 1665
(Reinikka, 1995). Wind orchids were particularly popular among warlords and samurai during the Edo
period (1603–1868) in Japan and was thus often called
the “Samurai orchid” or “Fuukiran,” meaning orchid
of the rich and noble. In this period, owning the
unusual mutant wind orchid was highly fashionable,
and this motivated enthusiastic expeditions to hunt for
valued wind orchid mutant plants from their natural
habitats (Reinikka, 1995). Today, this passion for the
wind orchid lives on, with orchid enthusiasts in Korea
and Japan growing hundreds of different mutants of
wind orchids. Recent advances in mass propagation of
the wind orchid have made rare mutants widely
available and continuously adds new mutants to the
collection.
CHARACTERIZING THE MUTANT FLOWER
MORPHOLOGIES OF THE WIND ORCHID
The wind orchid has a typical zygomorphic orchid
flower form, with two whorls of tepals and a central
gynostemium. The outer whorl consists of three similarly shaped outer tepals, whereas the inner whorl has
two inner tepals and one highly modified labellum (lip
tepal) with a long spur protruding from the abaxial
side of the labellum (Fig. 1, A and B). The gynostemium
(column), a reproductive organ with fused male and
female organs, is positioned in the center and terminates the floral axis. The mutants reported here share
peculiar flower forms and can be categorized into five
major groups: 1) homeotic changes of floral organs, 2)
increased or decreased organ number, 3) degenerated
floral organ development, 4) changes in the determinacy of the flower, and 5) altered spur development.
The spur mutants presented in Figure 2 can be further
categorized into three characteristic groups: 1) altered
spur length and curvature, 2) altered spur labellum
patterning and positioning, and 3) absent or ectopic
spurs.
Several wind orchid mutants show homeotic changes
in lateral organs. One of the most evident is a homeotic change between the labellum and an inner tepal
seen in the Geum-sung (Golden star) mutant (Fig. 1C).
In contrast to Geum-sung, Ok-hyang-ro (Jade incense
burner) converts each inner tepal into a labellum
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Neofinetia, Orchid Flower Mutant Collection
(Fig. 1D). Notably, the conversion between a labellum
and an inner tepal causes the disruption of floral
zygomorphy, and these mutants form perfectly radially symmetrical flowers. Given that the spur is
formed on the labellum, any substitution between a
labellum and an inner tepal also affects the number of
spurs in a flower. Thus, instead of the one spur seen in
wild-type flowers (Fig. 1B), Ok-hyang-ro generates
three spurs (Fig. 1D), while Geum-sung has no spur
(Fig. 1C).
Additional or missing floral organs have been found
in several mutants. Go-ya-ji-hwa, for example, has
fewer tepals and no labellum compared to wild-type
flowers (Fig. 1E). Most Go-ya-ji-hwa flowers have only
three outer tepals, although occasionally flowers form
between two and six tepals. Another mutant, Guigong-ja (Noble man), has three outer tepals and one
labellum but lacks any inner tepals (Fig. 1F). Sang-a
(Ivory tusk) has a normal number of tepals but forms
an additional labellum. The name is derived due to the
presence of an extra spur, causing the flower to resemble an elephant face with tusks (Fig. 1G).
Other mutants show flowers with degenerated floral
organ development. Some of the best examples are
Hong-bi-jeob (Red flying butterfly; Fig. 1H) and Ho-jeobji-mu (Butterfly dance; Fig. 1I). In these mutants the
tepal development is defective. In Hong-bi-jeob, the
labellum and two inner tepals develop normally, but
the three outer tepals show arrested growth. In particular, the growth arrest can be seen in the dorsal half
of two ventral outer tepals (Fig. 1H, v-o) and in the
distal part of the dorsal outer tepal (Fig. 1H, d-o). In
Hong-bi-jeob, all tepals acquire a leaf-like identity, with
the growth of each tepal arresting at a scale-like
structure, whereas the labellum develops normally
(Fig. 1I).
In the wild-type wind orchid, formation of the
gynostemium terminates the floral axis (Fig. 1A).
This floral determinacy is lost in some mutants (Fig.
1, J–N), where the continued meristematic activity in
Figure 1. Floral morphologies of wind orchid mutants and schematic diagrams of flowers (insets). A and B, A frontal (A) and side
(B) view of the wild-type wind orchid flower. C and D, Mutants with a homeotic conversion of floral organs from a labellum to an
inner tepal (C) and vice versa (D) with near-radial floral symmetry. E–G, Mutants with decreased (E and F) or increased (G) floral
organ number. H and I, Mutants with degenerative tepal development. J to N, Flower determinacy mutants. These mutant flowers
maintain meristematic activity and continue to produce tepals (J), leaf-like tepals (K), tepals and labella (L), or labella (M and N).
i, Inner tepal (colored purple in the diagrams); o, outer tepal (gray in the diagrams); la, labellum (white in the diagrams); g,
gynostemium; s, spur; pe, pedicel; d-o, dorsal outer tepal; v-o, ventral outer tepal. Bars = 3.00 mm.
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Duttke et al.
Figure 2. Spur morphologies of wind orchid mutants and schematic diagrams (insets). A, A wild-type flower with the spur
protruding in the abaxial side of the labellum. B to E, Mutant flower with no (B), a short (C), a long (D), and a highly coiled spur
(E). F to J, Spur patterning mutants. F, A mutant flower with the spur growing out from the adaxial (ad) side of the labellum. G, A
flower with inverted ab-adaxiality of the labellum. H, A flower with an additional spur growing in the adaxial side of labellum as
well as an abaxial spur. I and J, Mutant flowers with labellum positioned in the distal side of the spur. K to M, Mutants with three
spurs. K, Three spurs due to the conversion of the inner tepal to labellum. L and M, A mutant flower with two ectopic spurs
growing from the inner tepals (L) or two ventral outer tepals (M). Organs with spurs labeled with orange asterisks in the diagrams
in K to M. I, Inner tepal; o, outer tepal; la, labellum; s, spur; pe, pedicel; ab (colored in lavender), abaxial side of labellum; ad
(colored in green), adaxial side of labellum. Bars = 3.00 mm.
the center of the flower produces additional lateral
organs. The type of lateral organs produced varies
between the mutants. The indeterminate meristematic
center of the Nam-geuk-ji-mu (Fig. 1J) and the San-chuijun (Fig. 1K) flowers continuously generate tepals.
Although Nam-geuk-ji-mu produces normal-looking
tepals, San-chui-jun generates leaf-like tepals showing
chimerical features between the leaf and the tepal. In
Choon-geub-jeon, the flower meristem keeps generating
tepals and labella (Fig. 1L). It appears that each
gynostemium is substituted by an individual flower,
creating a Russian doll-like phenotype. Sa-man-sib-jahwa (Fig. 1M) and O-de-mo-yang (Fig. 1N) mainly
generate labella but occasionally produce scale-like
tepals. All indeterminate flower mutants can be further categorized into two groups: one group with the
elongated floral axis between lateral organs (Fig. 1, J, L,
M) and a second group without the elongated floral
axis between lateral organs (Fig. 1, K and N).
The wind orchid mutant collection also includes a
wide variety of spur mutants. The wild-type spur is
about 5 cm long and slightly curved (Fig. 2A). Choodong exhibits normal labellum and tepal morphology
but fails to develop a spur (Fig. 2B). This is distinct
from the Geum-sung flower (Fig. 1C), which also lacks a
spur but due to a substitution from the labellum to a
tepal. Other mutants exhibit variations in spur length.
The No-gye flower has a severely reduced (about 1 cm
long) spur (Fig. 2C), whereas the spur of Baek-ryung
reaches a length of 7 to 10 cm (Fig. 2D). The curvature
of the spur varies among mutants from straight to
highly coiled as seen in Hwang-joa-ji-mu (Fig. 2E).
Patterning or positioning of the labellum and spur is
altered in a number of mutants. In the wild-type
flower, the spur develops from the abaxial side of the
labellum (Fig. 2A). In contrast, in Chun-shim, the spur
develops from the adaxial side of the labellum (Fig.
2F). The flower of Byen-gyung-ji-hwa (Fig. 2G) is su-
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Neofinetia, Orchid Flower Mutant Collection
perficially similar to that of Chun-shim (Fig. 2F). However, the adaxial and the abaxial sides of the labellum
are inverted in Byen-gyung-ji-hwa (Fig. 2G). In the
Yong-seol-jo flower, two spurs develop from both adaxial and abaxial sides of the labellum (Fig. 2H). The
position of the labellum is altered in Mo-jung and Sulki-yi-jak, where the labellum is positioned in the middle (Fig. 2I) or the distal end of the spur (Fig. 2J).
Several mutants have flowers with three spurs. A
conversion from the inner tepals to labella generates
three labella and three spurs (Fig. 2K, Ok-hyang-ro).
Another route to creating three spurs without extra
labella is through ectopic spur formation on tepals.
Two mutants possess flowers with one labellum and
three spurs. A recently reported Korean mutant, Samkac-san (Mt. Triangle), has three spurs, with two ectopic spurs growing from the abaxial side of the inner
tepals (Fig. 2L). In Hwa-guye, two ectopic spurs grow
from the two ventral outer tepals (Fig. 2M).
EXPLOITING THE WIND ORCHID
MUTANT COLLECTION
To understand orchid flower evolution and development, it is necessary to determine the underlying
molecular mechanisms. The rich and constantly expanding collection of wind orchid flower mutants
provides a unique and useful tool for dissecting the
manifold aspects of orchid flower development as well
as flower evolution in other angiosperms. These include floral zygomorphy, floral organ pattern formation, and spur development. Recruitment of floral
zygomorphy is one of the key steps of orchid evolution
(Rudall and Bateman, 2002). Basal orchid genera, such
as Apostasia and Neuwiedia, with hexamerous radial
flowers (three inner tepals), have acquired floral zygomorphy by altering the ventral inner tepal into a
labellum along with stamen suppression (Bateman
and Rudall, 2006). Geum-sung, an atavistic mutant (Fig.
1C), and Ok-hyang-ro, a mutant with three labella (Fig.
1D), will provide key information for understanding
the radial-to-zygomorphic transition in orchid flowers.
Several studies report that the TCP transcription factor
CYCLOIDEA, a key regulator in establishing floral
zygomorphy in several dicot species (Cubas et al.,
1999; Hileman et al., 2003; Citerne et al., 2006; Feng
et al., 2006; Busch and Zachgo, 2007; Broholm et al.,
2008; Kim et al., 2008; Zhang et al., 2010), may also be
involved in orchid flower development (Rudall and
Bateman, 2002; Rajkumari and Longjam, 2005). Currently, however, there is no direct evidence indicating
that TCP genes are involved in orchid floral zygomorphy. It has been suggested that combinations of different B function MADS-box paralogs (APETALA3-LIKE
and PISTILLATA-LIKE genes) determine tepal and
labellum identities, termed “orchid code” (Tsai et al.,
2004; Mondragón-Palomino and Theissen, 2008, 2011;
Tsai et al., 2008). The role of MADS-box genes and the
orchid code hypothesis can be rigorously tested uti-
Figure 3. Phylogenetic relationship and spur morphology of the wind
orchid and closely related orchid species (adapted from Topik et al.,
2005). The short spur status (clades in black) evolved from the ancestral
long spur status (clades in purple). Later, several recruitments of long
spur (clades in purple) and no spur (clades in blue) occurred independently.
lizing the wind orchid mutants with altered tepal
identities and patterning. In addition, studying A and
C MADS-box genes (APETALA1 and APETALTA2,
AGAMOUS), LEAFY, SUPERMAN, and WUSCHELAGAMOUS pathways in mutant flowers with altered
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Duttke et al.
floral patterning and determinacy (Fig. 1, E–G, J–N)
will contribute to our understanding of pattern formation and organogenesis in petaloid monocots. Furthermore, this will also help to resolve the homology
among orchid tepals, grass floral organs, and dicot
petals/sepals, which will shed new light on flower
development and evolution in angiosperms as a
whole.
The spur is suggested to be one of the key innovations that led to rapid species diversification in many
plant lineages (Hodges, 1997; Bell et al., 2009). Darwin
hypothesized that the long spur of an orchid, Angraecum sesquipedale, was an outcome of an elaborate
coevolution with the proboscis length of its insect
pollinator (Darwin, 1877). The pollinator involved was
found in Madagascar about 40 years later (Rothschild
and Jordan, 1903). Despite its long history of interest,
to date, very little is known about the molecular
mechanisms underlying orchid spur development
and evolution. Analysis of the phylogenetic relationship of the wind orchid and closely related orchid
species showed that the prevailing short spur (,3 cm)
status (Fig. 3, clades in black) evolved from the ancestral long spur (.3 cm) status (Fig. 3, clades in purple).
Subsequent recruitments of a long spur (occurring
twice, including in the wind orchid, clades in purple)
and/or loss of the spur (Fig. 3, clades in blue) occurred
independently (Topik et al., 2005). The roles of the
KNOX genes, HIRZINA and INVAGINATA, in spur
development have been reported in snapdragon (Antirrhinum majus) and Linaria vulgaris, respectively
(Golz et al., 2002; Box et al., 2011). Studying these
KNOX genes as well as lateral organ adaxial-abaxial
polarity genes such as YABBY, KANADI, REVOLUTA, and PHABULOSA in the wind orchid spur mutants (Fig. 2) will shed light on our understanding of
orchid spur development such as positioning and
patterning.
WIND ORCHID AS A PROMISING ORCHID
MODEL SPECIES
With the long-standing historical interest and recent
development of orchid research, a need for an orchid
model species is pressing. An orchid model species
facilitates integrated research and enables us to focus
common resources, which will accelerate orchid research. The wind orchid has an immense potential as
an orchid model species. The wind orchid mutant
collection has been established over several centuries
and covers a wide range of mutant phenotypes, all of
which are readily available. These include mutants
with defects in flower lateral organ patterning, organogenesis, floral determinacy, floral zygomorphy, and
spur development. In particular, the range of spur
mutants exceeds any other plant species. Moreover,
the wind orchid offers even greater collections of
flower color, leaf shape, and leaf color (variegated
pattern) mutants. The mutant collection often contains
several independently occurring mutants exhibiting
identical or similar phenotypes, providing an invaluable resource that no other orchid species can offer.
Along with this collection, the wind orchid has several
other advantages over other orchid species. The wind
orchid is easy to grow and is amenable to producing
flowers under laboratory conditions. It is of small
stature (5–10 cm), allowing up to 100 plants to be
grown within a square meter. Tissue culture methods
for clonal propagation and optimized germination
systems are well established in the wind orchid
(Chung, 1979; Ichihashi and Islam, 1999; Islam and
Ichihashi, 1999). Agrobacterium-mediated transformation of the wind orchid further enables functional
analyses utilizing transgenic plants (Niimi et al., 2001).
The wind orchid is diploid (2n = 38) and has a
relatively small genome size (1C = 2.35 pg, about 6
times bigger than Arabidopsis) among orchids (Leitch
et al., 2009). Both selfing and outcrossing are possible
and a crossed flower yields thousands of seeds,
allowing genetic analyses in different mutant backgrounds (Chung, 1979; Arditti, 1992). Currently, the
most promising way to utilize the wind orchid mutant
collection is a candidate gene approach. This will be
accelerated by the ongoing development of deep sequencing and transcriptome analyses. With decreasing
costs of whole-genome sequencing (Drmanac, 2011),
even forward genetic approaches may be possible in
the long term. Subsequently, findings from the wind
orchid can be translated to closely and distantly related orchid species, providing genetic toolkits with
which to dissect the morphological diversity among
orchid species. Exploiting this extensive mutant collection with combined molecular and ecological
approaches will advance our understanding of development and evolution of the extraordinary morphologies, as well as the unique plant-animal and
plant-fungus interactions, found in the orchid family.
Furthermore, orchids represent an important petaloid monocot group, distinct from the majority of
wind-pollinated monocot flowers with sepal-like floral organs such as lemma and lodicules. Studies on
the wind orchid will thus advance our understanding
on angiosperm flower development and evolution in
broad terms.
ACKNOWLEDGMENTS
We thank the Korean Neofinetia Club “Pungppamo” (www.pungnan.com)
and Mr. Kook Hyung Han for providing the photos of the mutants and Dr.
Liz Sheffield, Dr. Patrick Gallois, Dr. Giles Johnson, Dr. Thomas Nuhse, and
Dr. Rebecca Wright for critical discussion of the manuscript.
Received December 7, 2011; accepted January 31, 2012; published February 1,
2012.
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